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The Global Epidemiology, Public Health Outcomes, Management, and Prevention of Re-Emerging Ectoparasitic Diseases

The Global Epidemiology, Public Health Outcomes, Management, and Prevention of Re-Emerging Ectoparasitic Diseases

Tropical Medicine and Health Vol. 36 No. 1, 2008, pp. 1-10 Copyright! 2008 by The Japanese Society of Tropical Medicine １

Review The Global Epidemiology, Public Health Outcomes, Management, and Prevention of Re-Emerging Ectoparasitic

James Herry. Diaz＊ Accepted 9 January, 2008

Abstract. The ancient ectoparasitic diseases share many features in common with newly emerging infectious dis- eases, such as Lyme , including hyperendemic causative agents afforded selective advantages by changing ecological or socioeconomic conditions; origination as zoonoses; transmission by competent vectors; and introduction into new, susceptible host populations. Many ectoparasites are also developing increased resis- tance to medical , including the safest . Over the past two decades, there have been several re- ports of outbreaks of ectoparasitic diseases, principally , , and , both in regional communi- ties and in travelers returning from developing nations. Today ectoparasitic diseases infest not only executives and tourists returning from travel to developed and developing nations, but also individuals immunocompromised by advancing age and institutionalization, chronic infectious and malignant disease, malnutrition and homelessness. Ectoparasitic diseases are no longer of children and socioeconomically disadvantaged populations in tropical countries; they have re-emerged as unusual, but not uncommon, infectious diseases worldwide. Key Words: Ectoparasites; Infestations, arthropod; Infectious diseases, emerging and re-emerging.

ology of ectoparasitic diseases in order to determine THE GLOBAL EPIDEMIOLOGY,PUBLIC HEALTH the factors responsible for their re-emergence and to de- OUTCOMES, AND PREVENTION OF RE-EMERGING velop effective strategies for the control and prevention of ECTOPARASITIC DISEASES community outbreaks. Today most areas of the world are accessible within 36 hours by commercial air travel [1]. As a result, interna- MATERIALS AND METHODS tional tourism to subtropical and tropical areas of both resource-poor and developed nations has tripled over the To chronologically evaluate the changing global epide- past two decades [1]. As national economies expand and miology of tropical ectoparasitic diseases and to determine personal incomes rise, there will be even more professional the human and environmental factors responsible for the re- time for business travel and more leisure time for vacation emergence of infectious ectoparasites with increased thera- travel to exotic locations, especially to regions with natural peutic resistance, data was extracted from both Medline attractions and pleasant climates. Several authors have now (National Library of Medicine) and Cochrane Review (The reported significant outbreaks of ectoparasitic diseases, Cochrane Collaboration, Oxford, UK) search engines, principally myiasis, scabies, and tungiasis in developing na- 1966-2007, of case reports, case series, descriptive epidemi- tions and in travelers returning from developing nations [1- ological investigations, analytical and pharmaceutical stud- 5]. In addition to these ectoparasitoses, the worldwide ies, and reviews of ectoparasitic diseases among both re- prevalence of other human ectoparasitic diseases is now in- gional populations and international travelers. creasing without regard to national economic development, including , myiasis, and other , , and THE EPIDEMIOLOGY OF EMERGING INFECTIOUS DISEASES miscellaneous arthropod infestations, such as bed bugs [1, 6]. This review will examine the evolving global epidemi- With the exception of pediculosis and scabies, most

*Corresponding author: Program in Environmental and Occupational Health Sciences, School of Public Health, Louisiana State University Health Sciences Center, New Orleans, Louisiana USA. 2021 Lakeshore Drive, New Orleans, LA 70122. Tel: 504-280-1600 Fax: 504-280-1516 E-mail: [email protected]. ２ human ectoparasitic diseases are caused by zoonotic dis- mens identified, there were 27 , 24 , 15 miscellane- eases (e.g., myiasis, tungiasis), and most are arthropod- ous , and 7 [1]. Most of the arthropod derma- borne (pediculosis, scabies, myiasis, tungiasis). The most toses originated in the UK (n = 46, 63%), and were caused commonly encountered arthropod ectoparasitoses and their by bites (n = 18), principally Ixodes ricinus (the com- clinical manifestations are featured in Table 1. mon tick), an important European vector of Lyme Ectoparasitic diseases share many of the characteristics disease and neuroborreliosis [1]. Myiasis cases predomi- of currently emerging infectious diseases, such as Lyme dis- nated in returning travelers (n = 18, 67%), principally fu- ease and West Nile virus, and even re-emerging infectious runcular myiasis from larval by an- diseases, such as leptospirosis and tularemia [7, 8]. Com- thropophaga (n = 9), the Tumbu , or monly shared characteristics of both ectoparisitoses and (n = 4), the human [1]. Among the arthropod derma- emerging infectious diseases include: (1) origination as toses caused by miscellaneous insects, most were due to zoonoses with disease establishment dependent on caused by infestation with Phthirus pubis, vector competency; (2) introduction into new, susceptible the pubic (n = 7), or to hemorrhagic, bullous bite host populations; (3) by endemic agents afforded groupings caused by lectularius, the common bed- selective advantages by changing ecological and socioeco- bug (n = 3) [1]. Among bedbug bite cases, there were 2 in- nomic conditions; and (4) movement from rural to urban digenous cases, and 1 case in a traveler returning from Italy endemic areas, usually following migrating human host [1]. The authors concluded that exotic infestations, particu- populations seeking better economic opportunities [7, 8]. larly myiasis, predominated in returning travelers from Af- Ectoparasitic diseases also share several specific eti- rica and , while pubic lice were domestic in- ological emergence factors with both emerging and re- festations, and infestations were both domestically emerging infectious diseases including: (1) the influence of and internationally acquired [1]. human behavior on subsequent ; (2) the effect of Recent epidemiological evidence now supports the en- parasite genetic adaptation and change on therapeutic drug demicity of several ectoparasitic diseases and their arthro- resistance; (3) the impact of international travel and the pod vectors and human and reservoir hosts through- globalization of trade and commerce on disease dissemina- out the developing world and in many parts of the devel- tion; (4) the breakdown of local public health infrastruc- oped world, including Europe. Ectoparasitic diseases have tures; and (5) the increasing urbanization of the world’s also re-emerged in regions where they were once effectively population with more inner city crowding in low-income controlled, such as in , , and the Caribbean. housing [7-9]. Some recent specific examples of emergence Ectoparasitic diseases will continue to re-emerge in the de- factors shared by ectoparasitic diseases and emerging infec- veloped world for several reasons including (1) the globali- tious diseases include: (1) promiscuous sexual behavior zation of trade and commerce with ectoparasites and even spreading the sexually transmitted ectoparasitic diseases, their rodent hosts traveling worldwide on container ships scabies and pubic lice, or pediculosis pubis; (2) microbial and cargo airplanes; (2) the worldwide legitimate and illegal adaptations resulting in multi- resistant Pediculus trade of exotic ; (3) the accidental and intentional humanus capitis (head lice); (3) furuncular myiasis in trav- introduction of exotic animal species into new regions; and elers returning from tropical vacations, and (4) a resurgence (4) the growing populations of accessible, and, often im- of scabies and tungiasis in both developing and developed munocompromised human hosts, living in crowded urban nations with languishing public health infrastructures, par- communities and mega-cities [6-10]. ticularly stray domestic animal and rodent control programs.

THE EPIDEMIOLOGY AND PUBLIC HEALTH THE EPIDEMIOLOGY OF RE-EMERGING OUTCOMES OF SPECIFIC RE-EMERGING ECTOPARASITIC DISEASES ECTOPARASITIC DISEASES To assess the potential combined impact of increasing Pediculosis Pediculosis is a complex of three different hu- international travel and the relaxation of quarantine regula- man infestations with two species of blood-sucking lice of tions for imported animals in the United Kingdom (UK) on the insect suborder Anoplura, Pediculus humanus and arthropod-induced dermatoses, McGarry and colleagues de- Phthirus pubis. After early man began to wear clothes, scribed their analyses of 73 insect specimens removed from Pediculus humanus evolved into two clinically distinct ec- symptomatic patients and submitted to their laboratory for toparasitic variants, P. humanus corporis, the , expert identification at the Liverpool School of Tropical and P. humanis capitis, the . Although morpho- Medicine, during the years 1994-2000 [1]. Of the 73 speci- logically indistinct, these human lice variants do not inter- ３ breed and prefer unique anatomic niches on their human nomic status, and primarily infest the indigent homeless, hosts. Pediculosis capitis, or head lice, is the most common refugees from civil unrest, or the immunocompromised. type of pediculosis, afflicting millions of people annually, Body and head lice are transmitted by direct contact be- mostly school-aged children, in both developing and indus- tween infested individuals, and, much less commonly, by trialized nations. Body lice infestations, or pediculosis cor- indirect contact with fomites, such as bedding, clothing, poris, are associated with poor hygiene and low socioeco- headgear, combs and brushes. Pubic lice are usually trans-

Table 1. Common Arthropod Ectoparasites and Common Names of Geographic Clinical taxonomy Representative Species of Infesting Distribution of of the Arthropod-borne Infesting Arthropods Arthropods Ectoparasitoses Class Insecta Order Phtiraptera Suborder Anoplura Lice Pediculus humanus corporis Body louse Worldwide Pediculus humanus capitis Head louse Worldwide Pediculosis capitis Phthirus pubis Crab (pubic) louse Worldwide Pediculosis pubis (phthiriasis) Order Diptera Flies Family Auchmeromyia senegalensis Congo floor- fly Sub-Saharan , Cape Verde Larvae are nocturnal blood Islands feeders, no myiasis Callitroga americana American screwworm North & Central America (cutaneous) myiasis Chrysomyia bezziana Old World screwworm Tropical Africa, Asia, Indonesia Cavitary (invasive) myiasis hominivorax New World screwworm Central America Cavitary (invasive) myiasis Tumbu (mango) fly Africa Furuncular myiasis Family Oestridae Cuterebra spp. Rodent botfly North & Central America Furuncular myiasis Dermatobia hominis Human botfly Central & South America Furuncular myiasis Order Heteroptera True bugs Cimex lectularius Common bedbug Worldwide Hemorrhagic bullous bite lesions Cimex hemipterus Tropical bedbug Subtropical and tropical areas Hemorrhagic bullous bite lesions. worldwide Potential vectors of , hepatitis B, and Tsukamarella spp. infections. Order Siphonaptera Ctenocephalides spp. Cat & dog fleas Worldwide Bite groupings (mechanical vec- tors of dog & rat tapeworms) Pulex irritans Human flea Worldwide Bite groupings (plague vector in Chilean Andes) Chigoe (jigger) flea Central & South America, Tungiasis Africa Xenopsylla cheopis Oriental rat flea Europe, Asia, Africa, Most efficient bubonic plague vector Class Arachnida Order Acarina Mites & ticks (scabies) mite Worldwide Scabies Trombicula alfreddugesi Common chigger (redbug) Worldwide Chiggers Trombicula akamushi Asian rodent chigger Worldwide Potential scrub vector Trombicula deliensis Indian rodent chigger Southeast Asia, Australia, Indo- Potential scrub typhus vector Pacific Islands ４ mitted during sexual contact, and often coexist with scabies the differential diagnosis of draining cutaneous lesions in and other sexually transmitted diseases. patients returning from tropical or exotic locations [20]. Unlike head lice and pubic, or crab, lice, body lice can Also in 1995, Gordon and coauthors reported 6 patients re- transmit several bacterial diseases. Homeless and refugee turning from Belize with furuncular myiasis from larval in- populations are at greatest risks of body lice infestations festation with Dermatobia hominis, the human botfly [21]. and epidemics of louse-borne bacterial diseases including: The authors concluded that botfly myiasis was occurring (1) caused by Borrelia recurrentis,(2) more commonly in travelers returning from the American caused by Bartonella quintana, (3) epidemic tropics, even from economically developed countries such typhus caused by Rickettsia prowazekii, (4) bacillary an- as Belize [21]. giomatosis caused by Bartonella henselae and Bartonella In 2003, Tamir and coauthors reported two Israeli trav- quintana, and (5) subacute bacterial endocarditis caused by elers returning from a 1-month trip to Ghana with furuncu- Bartonella elizabethae. Bartonella (formerly Rochali- lar myiasis from larval infestation by Cordylobia rodhani, maea) henselae and B. quintana have extensive domestic Lund’s fly [22]. The two patients had applied petroleum and wild animal reservoirs and have been recently recog- ointment to multiple draining lesions to partially suffocate nized as infectious organisms of high importance not only and dislodge the larvae, which were manually extracted a in displaced populations, but also in immunocompromised few days later [22]. The authors concluded that C. rodhani subjects, particularly individuals with the acquired immu- was an uncommon cause of furuncular myiasis compared to nodeficiency syndrome (AIDS) [8]. myiasis with Cordylobia anthropophaga (the Tumbu fly) Lice infestations remain very common in both the de- larval infestation in travelers returning from Africa and myi- veloping world and the industrialized world with a preva- asis with Dermatobia hominis (human botfly) larval infes- lence rate for pediculosis capitis, or head lice, exceeding tation in travelers returning from Central and South Amer- 25% in the elementary schools of industrialized countries ica [22]. The authors also warned that C. rodhani myiasis [6]. The prevalence of head lice is now increasing in South- could result in multiple furuncles, thus increasing the risks east Asia and the United States (US), and resistance to of or , and recommended that travelers to Cen- many commonly used pediculicides is increasing world- tral Africa avoid direct contact with sand to prevent C. rod- wide [6, 11-18]. Both Pediculus humanus (head and body hani myiasis, iron any clothes left outside to avoid C. an- lice) variants and Phthirus pubis (pubic lice) have now thropophaga (Tumbu fly) myiasis, and maintain their teta- demonstrated high levels of resistance worldwide to the saf- nus prophylaxis status [22]. est topical pediculicides, specifically the natural pyrethrins and the synthetic pyrethroids (, ) [11- Flea Infestations Fleas of the insect order Siphonaptera 19]. In addition, increasing resistance to , an or- are a small group of morphologically similar wingless ecto- ganophosphate insecticide, both alone and combined with parasites of warm-blooded animals that are not only biting pyrethroids, has been reported in the UK and elsewhere nuisances, but also competent vectors of infectious diseases, [17]. The escalating resistance of head lice to pyrethrins, most notably Yersinia pestis. Although fleas are often clas- pyrethroids, and malathion has led to an increase in the use sified by host specificity (or presence or absence of head of in treating drug resistant pediculosis capitis. Lin- combs), all fleas can rapidly adapt from animal to conven- dane is an organochlorine insecticide that bioaccumulates in ient human hosts, especially if preferred animal hosts are adipose and nerve tissue with over-application and can exterminated by disease or . Adult fleas can cause seizure activity, especially in children [6]. blood-feed on their hosts for up to a year, and can survive apart from their hosts up to 125 days [19]. Myiasis In 1994, Jelinek and coauthors, described 13 cases A currently re-emerging, combless ectoparasitic flea, of cutaneous myiasis in travelers returning from tropical Tunga penetrans, the chigoe or jigger sand flea, is endemic countries [20]. Of the 13 cases, 6 patients returning from in the Caribbean, Africa, and South America, where it origi- Africa presented with furuncular myiasis from larval infes- nated, and, especially, in sub-Saharan Africa, where it was tation with Cordylobia anthropophaga, the Tumbu fly; 6 introduced from South America in the late nineteenth cen- patients returning from the American tropics presented with tury [23-27]. Domestic animals, especially cats, dogs, , furuncular myiasis caused by Dermatobia hominis, the hu- and , and rodents are the major wild animal reservoirs man botfly; and one patient returning from Nepal presented for Tunga penetrans worldwide [2-5, 23-27]. with cutaneous myiasis due to infestation with Hypoderma Tungiasis, a painful, cutaneous infestation with the lineatum [20]. The authors concluded that myiasis should gravid female jigger flea, is a common nuisance in endemic be considered an increasingly common ectoparasitosis in regions of Africa, South America, and the Caribbean, and ５ has potentially serious sequelae, including tetanus, loss of summary, scabies is another re-emerging ectoparasitic dis- toenails, deformation and auto-amputation of digits [4, 23]. ease more often associated with crowding and homelessness Tungiasis has successfully re-emerged in Mexico and and immunocompromise by chronic infectious diseases, throughout Central America, where it was once controlled; such as AIDS and tuberculosis, than with poor personal hy- and has been increasingly reported in travelers returning giene. from subtropical and tropical areas worldwide [2-5, 23-27]. In 1996, Ibanez-Bernal and Velasco-Castrejon reported the THE GLOBAL EPIDEMIOLOGY AND PUBLIC HEALTH first new cases of tungiasis (n = 3) in Mexico since 1948, OUTCOMES OF ECTOPARASITIC INFECTIONS WITH with one infection acquired in Mexico City, a highly devel- -RESISTANT ECTOPARASITES oped, sophisticated metropolitan capital city [25]. In order to assess the current prevalence of several ec- Since the late 1980s, increasing resistance of head lice toparasitic infections in international travelers, Heukelbach to the most commonly prescribed pediculicides has been re- and co-authors recently conducted the first cross-sectional ported throughout the world [6, 11-17]. In Israel, head lice exit questionnaire study of 372 tourists returning home to resistance to permethrin increased four-fold between 1989 European countries after vacations in [5]. During and 1994 [6, 14]. Head lice resistance to natural pyrethrins, their stays in Brazil, 12 (3.2%) tourists contracted tungiasis permethrin, and lindane have been reported from Canada, and 3 (0.8%) tourists contracted cutaneous migrans, a the Czech Republic, Denmark, , Israel, the UK, and subcutaneous infestation with the larval hookworms of the US [6, 11-18]. Head lice resistance to malathion has dogs and cats, principally Ancylostoma braziliensis [5]. The been reported from the UK and from Africa [17]. length of stay in the host country was a significant predictor In a randomized comparison of wet-combing versus for tungiasis, with a 20 times higher occurrence in tourists 0.5% malathion for head lice in the UK, Roberts who remained in Brazil for more than one month [5]. The reported a 78% cure rate for malathion versus authors concluded that ectoparasitic infections were not un- 38% for wet-combing [6]. In an in vitro pediculicidal effi- common in international travelers exiting Brazil over a re- cacy comparison of 5 pediculicides available in the US, cent two-week study period, and that tungiasis was four Meinking and co-investigators reported the following re- times more common than cutaneous larva migrans [5]. sults: (1) there were significant differences in the pediculi- cidal efficacies of the 5 pesticides tested; (2) malathion was Mite Infestations Scabies, an infestation by the itch mite, the only tested pesticide in their study that had not become Sarcoptes scabiei, has remained a major public health prob- less effective as a pediculicide; (3) the ranked order of lem throughout the developing world, and has become a therapeutic effectiveness from most to least effective was significant re-emerging ectoparasitosis in its most severe 0.5% malathion, undiluted natural pyrethrins with piperonyl form, Norwegian or crusted scabies, in the industrialized butoxide, 1% permethrin, diluted natural pyrethrins with world, especially among the homeless and immunocom- piperonyl butoxide, and 1% lindane; and (4) some head lice promised. In rural areas of Central and South America, the in the US had become resistant to most pediculicides [28]. prevalence of scabies among children approaches 100% In a 2007 Cochrane Collaboration Review on the treat- [19]. In Bangladesh, the prevalence of scabies among chil- ment of scabies, Strong and Johnstone noted that both topi- dren exceeds the prevalence of both acute diarrheal diseases cal permethrin and oral appeared most effective and acute respiratory infections among children throughout for individual infections; more research would be needed to the year [19]. In Africa and Southeast Asia, where T-cell compare the effectiveness of malathion to permethrin for in- leukemia-lymphoma virus (HTLV-1) is prevalent, general- dividual infections; and there was insufficient evidence to ized crusted (Norwegian) scabies is often a heralding recommend specific miticides to control community and in- marker of adult T-cell leukemia or lymphoma [19]. Crusted stitutional outbreaks of scabies [29]. In short, there is re- scabies is now being diagnosed more commonly in home- cent evidence of increasing resistance of head lice to the less or displaced populations worldwide and in patients im- safest pediculicides, the natural pyrethrins and the synthetic munocompromised by human immunodeficiency virus pyrethroids, and more research will be required to deter- (HIV) infection and AIDS [19]. mine the best treatment strategies for controlling outbreaks Scabies is easily transmitted by skin-to-skin contact as of scabies. with sex partners, children playing, or even health providers Malathion, an organophosphate pesticide, has demon- examining highly infectious patients with crusted scabies. strated the greatest therapeutic efficacy against head lice in Scabies may also be transmitted by fomite contact with per- the US [28]. Carbaryl, a carbamate pesticide, highly effec- sonal grooming items, towels, clothes, and bed linens. In tive against both head lice and scabies, is being increasingly ６ prescribed for pediculosis capitis outside of the US, espe- topical or systemic treatments with pediculicides, 7-10 days cially in Europe and the UK. Lastly, therapeutic options for apart, and removal of all viable nits by carefully combing the control of scabies and crusted scabietic super- wet hair [6, 12, 18]. Olive oil, petroleum jelly, or Hair- infestations in community, institutional, and refugee shelter Clean 1-2-3! are preferred hair-wetting agents prior to outbreaks remain untested. combing [6, 12, 18]. Unfortunately, no ideal pediculicide Unfortunately, all of the topical pesticides used to treat with 100% killing activity against lice and nits exists [6, 12, ectoparasitic infections share the same three characteristics 18, 28]. Table 2 presents the most commonly used pedicu- as the three most commonly ingested childhood poisons. licides for lice infestations. As noted, drug resistance is in- They are (1) prescribed (often over-the-counter) medica- creasing to the safest pediculicides, the pyrethrins and syn- tions, (2) household products, and (3) pesticides. As the thetic pyrethroids, and to malathion, an organophosphate in- prevalence of ectoparasitic infections with pesticide- secticide with 95% efficacy against viable nits [6, 11-19, resistant ectoparasites in children increases, alternative pes- 28]. ticides, more toxic than pyrethrins and pyrethroids, may be Prevention strategies for head lice include combina- prescribed for ectoparasitic infestations; medications will tions of sanitizing the environment, and, more importantly, continue to be administered in households; and household eliminating all human reservoirs of head lice in households, accidental ingestions of more toxic pesticide formulations apartments and other housing complexes, classrooms, and for head lice and scabies may increase without enhanced schools [18, 29-31]. Some common preventive interven- public health education measures. tions include: (1) avoiding contact with potentially con- taminated items, such as hats, headsets, clothing, towels, combs, brushes, bedding, and upholstery; (2) soaking all THE CLINICAL MANIFESTATIONS,MANAGEMENT, combs and brushes in isopropyl alcohol or 2% Lysol! solu- AND PREVENTION OF RE-EMERGING tion; (3) sanitizing the household environment by high heat ECTOPARASITIC DISEASES cycle washing and drying of all bedding, clothing, and Pediculosis The clinical manifestations of pediculosis capi- headgear; and (4) inspecting high risk school children for tis range from asymptomatic infestation to severe pruritus active head lice and viable nits [6, 12, 18, 19, 29-32]. with self-inflicted, often secondarily infected, excoriations Prevention strategies for body and pubic lice are simi- with impetigo and postoccipital lymphadenopathy. The dif- lar and include: (1) hot cycle washing and drying of all ferential diagnosis of pediculosis capitis includes, eczema, clothing and bedding; (2) institution of basic personal hy- lichen simplex chronicus, dandruff, seborrheic dermatitis, giene and sanitation measures; (3) treatment of sexual con- and bacterial impetigo [19]. Management includes two tacts with active infestations; and (4) examination and labo-

Table 2. Recommended Pediculicide Treatments for Pediculosis Pediculicide Formulations Therapeutic Efficacy Safety profile Contraindications 0.33% pyrethrins + 4% 95% ovicidal. Excellent Chrysanthemum & daisy piperonyl butoxide shampoo No residual activity. (Plant Family Compositae) Increasing drug resistance. allergies 1-5% permethrin cream rinse 2-week residual activity. Excellent Prior allergic reactions Increasing drug resistance. 0.5% malathion lotion, 1% 95% ovicidal. Flammable Infants and children under malathion shampoo Rapid (5 min) killing. 78% isopropyl alcohol vehicle 6 months of age. (unavailable in USA) Good residual activity. stings , skin, and mucosa. Pregnancy Increasing drug resistance. Increasing drug resistance. Breast feeding Organophosphate poisoning risks with over-applications and ingestions. 1% lindane lotion and shampoo 95% ovicidal. Potential for CNS toxicity from Pre-existing seizure disorder. No residual activity. organo-chlorine poisoning, Infants and children under Increasing drug resistance. usually manifesting as seizures, 6 months of age. with over-applications and Pregnancy ingestions. Breast feeding Ivermectin, 200 mcg/kg single Excellent Excellent Safety in pregnancy uncertain. po dose, repeated in 10 days. Not recommended for children 0.8% shampoo weighing < 15 kg. (unavailable in USA) CNS: central nervous system. ７ ratory testing of patients and their sexual contacts for other Victims rarely recall a flying insect bite that preceded botfly sexually transmitted diseases, especially scabies and AIDS. -induced furuncular myiasis. While developing in their fu- runcles, larvae are active, protrude intermittently through Myiasis Myiasis is defined as human tissue invasion by the draining , and maintain surface contact for respira- dipterous larvae or of flies and may be classified tion with their posterior, paired spiracles. Anterior hooklets clinically as furuncular (subcutaneous) myiasis, wound (su- anchor the maggots in place subcutaneously, making man- perficial cutaneous) myiasis, cavitary (atrial or invasive) ual removal, even with forceps, difficult. myiasis, intestinal myiasis, urinary myiasis, and vaginal Management strategies for furuncular myiasis include myiasis. Relatively uncommon, intestinal myiasis is usu- coaxing embedded larvae to emerge from furuncles by cov- ally due to the accidental ingestion of maggot-contaminated ering their respiratory spiracles, often visible in lesions, food and is characterized by self-limited nausea, vomiting, with occlusive coatings of Vaseline! (petroleum) ointment, and diarrhea. Urinary myiasis is also uncommon and may clear fingernail polish, tobacco tar, pork fat, or, even, bacon present as dysuria, hematuria, and pyuria, following larval strips [21, 22, 33-35]. The injection of lidocaine into drain- invasion of the urethra, and/or vagina (vaginal myiasis). ing lesions has also been recommended as a successful ex- The most common forms of human myiasis are furun- traction technique [35]. Nevertheless, unsuccessful occlu- cular myiasis and cavitary or invasive myiasis. Furuncular sive may asphyxiate larvae and necessitate their sur- myiasis is often caused by subcutaneous larval invasion by gical extraction. Along with larval removal or surgical ex- the Tumbu fly, Cordylobia anthropophaga, in Africa, and traction, myiasis wounds should be cleansed and conserva- in subtropical and tropical areas of the Americas, tively debrided, tetanus prophylaxis administered, and bac- including the human botfly, Dermatobia hominis,and terial secondary infections treated with antibiotics. Preven- Cuterebra spp. botflies [20-22, 33-35]. Cavitary myiasis is tion and control strategies for myiasis include: (1) control usually caused by zoonotic screwworm larval deposition in of domestic and animal larval infestations; (2) open wounds or external orifices, such as the nares, , sanitary disposal of animal carcasses and offal to deny flies and orbits, and may be characterized by deep tissue larval their preferred breeding grounds; (3) proper management of invasion with secondary infection and extensive tissue de- any open human wounds or cutaneous infections; (4) ce- struction. , the New World menting floors to deny floor maggot flies their preferred screwworm, is a common cause of cavitary myiasis in the -laying surfaces; (5) sleeping on raised beds or cots in Americas; and bezziana, the Old World screw- screened huts or tents; (6) wearing long-sleeved shirts and worm, is a common cause of cavitary myiasis in Africa, pants, which can be pyrethrin-impregnated; (7) spraying ex- Asia, and Indonesia. Cavitary myiasis must be managed posed skin with diethyl toluamide-containing (DEET) re- aggressively with surgical débridement and antibiotic ther- pellants; and (8) ironing all clothes and diapers spread left apy of secondary infections to limit tissue damage. outside in Tumbu fly habitats [20-22, 33-34]. Although the clinical manifestations, treatments, and prevention strategies are similar in furuncular myiasis; the Flea Infestations Tungiasis is caused by the penetration of mechanisms of larval invasion are often different. The fe- the gravid female chigoe flea into the epidermis to feed on male Tumbu fly deposits its on moist soil or on wet blood and tissue juices, usually on the feet and under the clothing (e.g., cloth diapers) hung outside to dry. When the toenails or in the interdigital web spaces. The embedded human victim dons egg-infested clothing, larvae emerge flea will produce a subcutaneous papule or vesicle 6-8 mm and rapidly burrow into the skin with sharp mandibles for in diameter with a central black dot pinpointing the exteri- further development. On the other hand, the female botfly orized segments. The papule darkens with intralesional captures blood-feeding insects, usually mosquitoes, in mid- hemorrhage, and, if squeezed, will extrude eggs, , and flight, and attaches her eggs to the undersurface of the in- internal organs through exteriorized posterior abdominal sect. The intermediate biting vector then delivers the botfly segments. The differential diagnosis of tungiasis includes eggs to its blood meal victims, where the eggs hatch imme- staphylococcal skin infections, bacterial and fungal parony- diately and release their larvae to feed on warm-blooded chia, cercarial dermatitis, fire ant bites, and folliculitis [19]. hosts. The botfly larvae then rapidly burrow into the skin Management strategies for tungiasis include extracting with sharp mandibles in order to begin their developmental all embedded fleas immediately with sterile needles or cu- instar stages. After completing three instar stages, the final rettes, administering tetanus prophylaxis, and treating sec- larval forms of both the Tumbu fly and botfly will wriggle ondary wound infections with appropriate topical and/or out of their draining, -like furuncular swellings, drop to oral antibiotics. For heavy infestations, oral therapy for 3 the ground, and pupate into adult flies within 9-14 days. days with either thiabendazole (25 mg/kg/day) or albenda- ８ zole (400 mg/day) has been recommended [5, 19]. In addi- characteristic topographical distribution as 10-15 fertile fe- tion to wearing shoes, which can be sprayed with DEET so- male mites are transferred from infected patients to new lutions or dusted with 10% DDT powder, preventive strate- hosts. Female mites burrow into the thinner areas of the gies for tungiasis include: (1) insecticide treatment of flea- epidermis, usually no deeper than the stratum granulosum, infested domestic and stray animals and pets with 10% py- to lay their eggs at the end of tunnels 5-10 mm long. The rethrin spray, or 4% malathion powder; (2) foot bathing of preferred distribution of infestation includes hairless areas domestic and stray dogs and pigs with insecticide solutions; with a thin stratum corneum, such as the sides and interdigi- and (3) spraying or dusting households, especially those tal web spaces of fingers and toes, popliteal fossae, flexor with dirt floors, with 1-4% malathion. Other strategies for surfaces of the wrists, and buttocks. A more severe, often the environmental control of fleas include spraying rodent sexually transmitted sensitization reaction, nodular scabies, runways and paths and household walkways and floors with targets the external genitalia, particularly in males. solutions containing kerosene, fuel oil, 2% chlordane, 1% With primary infestations, the onset of pruritus and lindane, 3-4% malathion, 5% methoxychlor, or 1% trichlor- characteristic lesions are delayed up to 21 days, but follow- fon [2, 19]. Heukelbach has emphasized the importance of ing initial sensitization, symptoms and lesions return within controlling regional epizootic reservoirs of T. penetrans not 1-3 days of re-infestation. Characteristic lesions include only in domestic and stray dogs and cats, but also in domes- linear to serpiginous intraepidermal burrows, 5-10 mm long, tic pigs and cattle, and, especially, in rats [2]. Heukelbach dotted with fecal lithes or scybala and terminating in raised and co-investigators have described T. penetrans infesta- papules hiding ovipositing females. Diagnosis is confirmed tions in over 50% of rodents (Rattus rattus) captured in by microscopic examination of a burrow skin scraping poor communities in Brazil [2]. which excavates the female mite, (2- 0.5 mm in length), and surrounding eggs (0.02-0.03 mm) [19]. Scabietic nodules Mite Infestations Scabies presents as nocturnal itching in a will develop in 7-10% of patients with scabies, usually on

Table 3. Recommended Miticide Treatments for Scabies Miticide Formulations Therapeutic Efficacy Safety profile Contraindications 5% permethrin cream Apply from neck down; Excellent Prior allergic reactions wash off after 8-12 hours. Good residual activity. 1% lindane lotion or cream Apply from neck down; Potential for CNS toxicity from Pre-existing seizure disorder. wash off after 8 hours. organo-chlorine poisoning, Infants and children under No residual activity. usually manifesting as seizures, 6 months of age. Increasing drug resistance. with over-applications and Pregnancy ingestions. Breast feeding 10% crotamiton cream Apply from neck down on Excellent 2 consecutive nights; wash off Exacerbates pruritus. 24 hours after 2nd application. 2-10% in petrolatum Apply for 2-3 days then wash. Excellent Pre-existing sulfur allergy. 10-25% benzoyl benzoate 2 applications for 24 h with Irritant 1 day to 1-week interval. Exacerbates pruritus. Can induce contact irritant dermatitis. 0.5% malathion lotion, 95% ovicidal. Flammable Infants and children under 1% malathion shampoo Rapid (5 min) killing. 78% isopropyl alcohol vehicle 6 months of age. (unavailable in USA) Good residual activity. stings eyes, skin, and mucosa. Pregnancy Increasing drug resistance. Increasing drug resistance. Breast feeding Organophosphate poisoning risks with over-applications and ingestions. 2% sulfiram lotion Any ethanol consumption Ethanol consumption within within 48 hours of application 48 hours of application. may cause severe nausea and vomiting (the disulfiram effect). Ivermectin, 200-mcg/kg single Excellent Excellent Safety in po dose, repeated in 10 days.. Recommended for endemic or pregnancy uncertain. 0.8% lotion epidemic scabies in institutions Notrecommendedinchildren (unavailable in USA) and refugee camps. weighing < 15 kg. CNS: central nervous system. ９ the penis and scrotum, and appear as darkened, tender nod- Historically, bedbugs were regarded as potential me- ules 5-20 mm in diameter, often with a raised female mite chanical carriers but not as biological vectors of human in- burrow on top. fectious diseases. However, bedbugs can transmit Chagas Unlike typical scabies, crusted scabies spreads to the disease, caused by Trypanosoma cruzi, in endemic regions face, scalp, neck, and trunk, with the most heavily infested [38]. Although uncommon and unconfirmed microbiologi- areas capped by well-demarcated psoriatic-like plaques, cally, bedbugs may also transmit hepatitis B and Tsuka- which crust and scale. The differential diagnosis of scabies marella spp. (commensal in bedbug gastrointesti- is extensive and includes drug reactions, eczematous derma- nal tracts) infections during blood-feeding [39]. The most titis, fiberglass dermatitis, dermatitis herpetiformis, pedicu- commonly infesting bedbug species are listed in Table 1. losis corporis, lichen planus, and pityriasis rosea [19]. Recommended management strategies for scabies are CONCLUSIONS listed in Table 3. Prevention and control strategies for sca- bies include: (1) aggressive treatment of infested patients, The ectoparasitoses are no longer diseases afflicting especially those with highly infectious crusted scabies; (2) only barefoot children, displaced people, and socio- disposal or hot wash-dry sterilization of all contaminated economically disadvantaged residents of tropical countries. clothing and bedding; (3) provision of improved access for Human ectoparasitoses, such as, myiasis, scabies, and personal hygiene for all displaced, homeless, or institution- tungiasis, have now re-emerged as unusual, and often mis- alized persons; and (4) aggressive control of outbreaks of diagnosed, diseases among tourists, executives, missionar- zoonotic scabies caused by itch and mites of various ies, and soldiers from industrialized nations returning from domestic animals, especially cats, dogs, camels, pigs, and vacations or job-related assignments in locations throughout horses. developed and developing nations, including popular resort Although of limited clinical significance, a number of destinations. Ectoparasitic diseases are significant sources other mite species can cause bothersome dermatitis and of morbidity in , particularly children, and should even transmit infectious diseases, including scrub typhus, not be neglected as international outbreaks will continue to endemic typhus, and rickettsial pox [36]. The trombiculid occur with resistant strains that are difficult to control. species of chigger mites, or redbugs, can transmit scrub ty- Clinicians should be aware of the re-emergence of hu- phus caused by Rickettsia tsutsugamushi in North America man ectoparasitoses in order to make timely diagnoses and (Trombicula spp.) and in Southeast Asia, Australia, and the institute proper therapies ranging from surgical therapies for Indo-Pacific (T. akamushi, T. deliensis) [36]. Among the myiasis and tungiasis to topical and systemic therapies for chiggers, the adults and nymphs live in scrub brush and pediculosis and scabies. In addition, public health officials blood feed on rodents and small , and only the de- should be informed of regional ectoparasitic disease out- veloping larvae feed on humans when incidentally encoun- breaks in order to institute investigation, prevention, and tered. Rather then burrowing into the skin, chigger larvae control strategies to protect vulnerable populations, includ- insert their mouthparts or capitula into the skin to feed on ing executives, vacationers, missionaries, aid workers, refu- body fluids and epithelial cells that accumulate in a sty- gees, soldiers, long-term care residents, and the immuno- losome, a tube-like feeding reservoir created by the host’s compromised. inflammatory reaction to chigger saliva [36]. Chigger lar- vae feed on humans in the warmest topographic areas, espe- REFERENCES cially in areas of tight clothing, such as the ankles, axillae, waistline, and perineum. １．McGarry JW, McCall PJ, Welby S. 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